2004 Rapport 2004:1

Uptake of Organic Pollutants in Plants

Litterature survey

by

Anna Hellström

Department of Environmental AssessmentSwedish University of Agricultural SciencesBox 7050 SE 750 07 Uppsala

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Uptake of Organic Pollutants in Plants

ISSN 1403-977X

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INTRODUCTION................................................................................................ 7

UPTAKE FROM SOIL........................................................................................ 9

Remediation 14

UPTAKE FROM AIR........................................................................................ 15

Biomonitoring 19

TRANSPORT AND METABOLISM................................................................ 20

METHODS ......................................................................................................... 24

MODELS ............................................................................................................ 27

REFLECTIONS AND FUTURE RESEARCH ................................................ 28

REFERENCES................................................................................................... 30

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Introduction

Huge amounts of synthetic chemicals are constantly released into our environment. Man-made

chemicals are often referred to as anthropogenic (from Gr. Anthropos - a man, and genos - born of acertain kind) or xenobiotic (from Gr. xen (o) - strange, stranger, and biosis - way of life) since they

are foreign to nature. Distributed into different part of the environment chemicals can be transported

long or short distances and can also undergo a variety of reactions and transformations. Because ofthese many competing interactions the fate of such pollutants is not easy to predict.

Plants are the basal step in the terrestrial food web and are therefore central to both agricultural and

natural ecosystems. The same features that account for accumulation and concentration of dilute

resources also predispose plants for the accumulation of some anthropogenic substances. Thisuptake and concentration into a living organism from its environment is called bioconcentration

(Bernes, 1998). The bioconcentration factor (BCF) is defined as the ratio of the concentration of a

chemical in an exposed biological system to the concentration in the surrounding medium. If theconcentration of a chemical in an organism is dependent on both the concentration in the medium

and in the food the compound is said to bioaccumulate. Transfer of a pollutant from one trophiclevel to another leading to increased concentration is referred to as biomagnification. Although

investigations of aquatic systems are more common some studies have been done on

bioconcentration of hydrophobic chemicals in terrestrial food chains (McLachlan, 1996; Kelly &Gobas, 2001).

The pathway by which organic pollutants enter the vegetation is a function of chemical and physical

properties of each pollutant, such as hydrophobicity, water solubility, and vapour pressure, as well

as environmental conditions, such as temperature, organic content of the soil, and plant species.Uptake of organic chemicals into plants can occur from air or soil, depending on the properties of

the compounds. Foliage presents the largest plant area for uptake from air. Many of the mostproblematic pollutants are hydrophobic and the large lipid covered surface of leaves provides an

ideal sink for accumulation of these chemicals. Leaves, and to some extent shoots and stems,

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contain stomata through which gaseous molecules diffuse in and out and interact with a large

hydrophobic area.

Water is a key factor in most processes that take place in plants. It delivers mineral nutrients to the

shoot, transports photosynthesis products from the leaves, is responsible for turgidity and control ofthe openings for gas exchange (stomata), serves as substrate for biochemical reactions, and acts as

coolant. Water also serves as solvent, transport medium and reactant for uptake, translocation, anddegradation of anthropogenic chemicals in plant and soil. Water and solutes moves freely from soils

to the interior of roots in the capillary spaces between the outer layers of cells (cortex). The inner of

the root (stele), containing the transport vessels, is separated from cortex by a cell layer(endodermis) which in most roots contain the Casparian band; a waxy band acting as a barrier for

transport in cell walls and the intercellular space forcing all compounds to pass through the cellmembranes of endodermis (Hopkins, 1999). The area outside endodermis plays an important roll in

the movement of anthropogenic chemicals since this zone present an extensive surface for the

adsorption of pollutants (Trapp & McFarlane, 1995).

Transport in plants takes place in the two-vessel systems xylem and phloem. In the xylem fibrouscells provide support, parenchyma cells storage area for starch and fat, and in the main cells,

tracheary elements are responsible for most of the water transport in the plant. In mature plants

these tracheids are dead tissue. Water movement across the membrane is most properly described asdiffusion although an osmotic gradient also exists, favouring net movement of water in one

direction. Main conducting cells of phloem are the sieve elements that have functional membranes

and are filled with living protoplasm. There are however no intact nuclei or vacuoles in maturesieve cells. The solutes, which mostly consist of sucrose, are moved into phloem by an active

process requiring energy in the form of ATP. Solutes create osmotic gradients. Since nomechanism exists to keep non-ionic anthropogenic chemicals in the phloem sap, the concentration

will not exceed the concentration in the xylem (Trapp & McFarlane, 1995).

Plants have several mechanisms to protect them from uptake and transport of toxic substances.

Transport of the hydrophobic organic pollutants is limited in phloem by the nature of the chemical.Phloem and membrane transport is often not compatible because a hydrophobic compound that

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easily cross the membrane are not readily transported in the phloem. Anthropogenic chemicals can

also be rapidly degraded by active enzymes (Trapp & McFarlane, 1995). Soil sorption limits theavailability of chemicals for plant uptake. Photochemical reactions may degrade chemicals sorbed

to the leaves. A rapid flux of water flushes volatile pollutants to locations where they may leave the

plant.

Uptake of organic pollutants in plant has been reviewed. Paterson and co-workers (1990) reviewedthe mechanisms of uptake of organic chemical contaminants by plants from soil and air, based on a

compilation of 150 references documenting the fate of 70 chemicals in 88 species of plant and trees.

Simonich and Hites (1994) reviewed the recent studies of organic pollutant accumulation invegetation. A summary of published literature from the UTAB database pertaining to the

uptake/accumulation, translocation, adhesion and biotransformation of organic chemicals byvascular plants was made by Nellessen and Fletcher (1993). Trapp and MacFarlane (1995) have

summarised plant contamination by organic contaminants.

Uptake from soil

Organic pollutants can reach the soil by dry or wet deposition after either long-range aerial transport

from diffuse sources, or from short-range transport from point sources such as industrial discharges,

waste deposits, pesticide spraying etc. The contaminants are partitioned between, soil particles,interstitial water, and interstitial air, and uptake by plants may occur from the water or air phases.

The fate of a specific compound in a specific soil depends on the physical and chemical propertiesof both the compound and the soil. The most important property is hydrophobicity, which usually is

expressed as the 1-octanol/water partition coefficient (Kow), or more often log Kow. Log Kow spans

over a wide range for different organic compounds as can be seen in figure 1. To describe thedistribution of a chemical in soil the soil/water partition coefficient (Kd) is used. Kd is generally

proportionally to the hydrophobicity of the compound and to the amount of soil organic matter.

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The content of organic carbon in soil is one of the most important environmental factors influencing

root-uptake of non-ionic organic compounds from soil into roots. Sorption onto organic carbon Koc

can be determined from Kd:

Koc = Kd 100 / % organic carbon

More hydrophobic compounds, having a higher Kow, are sorbed more strongly to organic particlesin the soil. This is described in a linear relationship given by Briggs (1981)

log Kom = 0.52 log Kow + 0.62

Where Kom (sorption onto organic matter) is equivalent to Koc. Hydrophobic compounds, Kow>4,

will be strongly sorbed, Kd>10, and moderately hydrophobic compounds, Kow 2-4, moderatelysorbed, Kd = 1-10, in soils with organic contents of 1-5% (Trapp & McFarlane, 1995). In most

research on the uptake of organic contaminants into plants Koc is used. Dieldrin uptake in carrots

Figure 1 Ranges of octanol/water partition coefficients (as log Kow) for commonly occurring compounds invarious classes of pesticides and industrial pollutants. Asterisks indicate ionizable compounds whose log Kowvalues are plotted for the undissociated molecule. From (Trapp & McFarlane, 1995).

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Figure 2 Pathways of movement of xenobiotics to plants through soilas determined by Henry’s law constant. From (Trapp & McFarlane,1995).

from contaminated soil decreased significantly (more than ten times) when 20 % brown coal was

added (Bhattacharya & Douglas, 1997).

In soil compounds are also distributed between air and water. This partitioning is dependent on

vapour pressure and water solubility and is described by Henry’s law (Schwarzenbach, 1993):

KH = Pi/Cw or KH’ = Pi/(Cw* RT)

Where Pi is the partial pressure, Cw is the concentration in water, KH is the Henry’s law constant,

and KH’ is the dimensionless Henry’s law constant. A common way to determine KH’ is to calculateit from a compounds vapour pressure and water solubility (Trapp & McFarlane, 1995):

KH’ =T/273*(v.p*10-5)/(22.4 *W.S)

Where v.p. is the vapour pressure(Pa), W.S is the water solubility

(mol/l) and T the temperature (K).Compounds with high Henry’s law

constant will have a high

concentration in the vapour phaseand usually a low affinity for water

and they are predominately taken up

via the vapour phase and areunlikely to be translocated in plants

(Trapp & McFarlane, 1995).Pathways for compound with

different H’ are shown in figure 2.

Polar and anionic compounds move

in soil-water and their mobilityrelative the root affects uptake.

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Figure 3 Pathways for the movement of water from soil into thetrachery elements. From (Raven et al., 1992).

Cations are more strongly bond in soil, by the process of ion exchange, giving high Kd for simple

bases and even several orders higher for doubly-charged organic cations (Trapp & McFarlane,1995). Therefore uptake of ionised compounds is also affected by pH besides properties such as

hydrophobicity and organic matter. Uptake of weak acids normally increases when surrounding pH

decrease (Briggs, 1981). The non-ionic acid can pass the membrane dissociate to the anion in theplant compartment of higher pH and be trapped at that side of the membrane.

When entering the root with the

water stream a compound can

follow three possible pathways.The apoplastic pathway, via the

cell walls, the symplastic pathwayin the protoplasm via the

plasmodesmata, or the transcellular

pathway, from vacuole to vacuole(Raven et al., 1992). This is

illustrated in figure 3 showing aroot in section. The compound can

move in the, apoplast, and thereby

avoid entering the cells, until reaching the endodermis, a cylindrical sheet of cells that are tightlyconnected by the waxy, water impermeable Casparian band. There all molecules are forced to

traverse the plasma membranes and the protoplasts of the tightly packed endodermal cells and enter

the symplast to reach the xylem where they can be translocated. This barrier requires an activetransport for hydrophobic compounds (Trapp & McFarlane, 1995). There is also a possibility of

transport with resin or latex flows.

The efficiency of uptake by roots can be described as the ratio between concentration of chemical in

roots and the concentration in the surrounding medium. This is called the root concentration factor(RCF). Brigg and co-workers (1982) showed that uptake of nonionised compounds consists of two

components (1) an equilibration of the concentration in the aqueous phase inside the root with theconcentration in the surrounding solution (0,82 of RCF) and (2) sorption on hydrophobic root

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solids. The latter component seems to become important above log Kow of 1.5. In barley, Brigg’s et.

al. established the following relationship for carbamoyloximes and phenylureas:

log(RCF-0.82) = 0.77 log Kow - 1.52

This relationship was found to hold for uptake of a range of non-ionised compounds by a variety of

plant species (Briggs et al., 1982).

Many studies have been performed to investigate the plant uptake of hydrophobic compounds like

polychlorinated biphenyls(PCBs), dioxins (PCDD), furanes (PCDF) and polycyclic aromatichydrocarbons (PAHs) from soil. Most of the studies in greenhouse (O'Connor et al., 1990), and in

field (Fries & Marrow, 1981; Sawhney & Hankin, 1984; Webber et al., 1994) of uptake of PCB,dioxins, DDT and other hydrophobic compounds from soil have shown that the only root uptake

that can be seen are accumulation in the lipid-rich peels of e.g. carrot, beet and turnip. There is

almost no strong evidence of transport in plants to above ground parts. No translocation of eitherphenols or PAHs to grain of barley grown on soil treated with two kinds of contaminated fertilisers

was found by Kirchmann & Tengsved (1991). Plant uptake 2,4,6-trichlorophenol is probably nomatter of concern in soils contaminated with low concentrations according to a study by Sceunert

and co-workers BCR was lower than 1 for carrot, cress, maize, and beans and 2.5 for barley

(Scheunert et al., 1989). Roots of hydroponically grown soybean and corn adsorbed 70 % of addedlabelled TCDD in a laboratory study, but no translocation was detected (McCrady et al., 1990).

Thus, contamination of leaves and shoots seems to be due to uptake from air in most cases (Fries &

Marrow, 1981; Bacci & Gaggi, 1986; O'Connor et al., 1990; Webber et al., 1994; Heinrich &Schulz, 1996).

There is, however, one interesting exception. Hülster and co-workers found active transport of

dioxins in two members of the genus Cucurbita, zucchini (Cucurbita pepo L. cv. Giromontiina) and

pumpkin (Cucurbita pepo L. cv Gelber Zentner) (Hülster et al., 1994). Cucumber (Cucumis sativus

L. cv Delikatess), which, like zucchini and pumpkins, belongs to the family of Cucurbitaceae did

not show any uptake of dioxins from soil. This behaviour is not yet fully understood. Some morestudies on uptake of chloro-organic compounds in Curcubita (White et al., 2003) and other crops

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(Mattina et al., 2000) has been published. The case is different with many “modern” pesticides.

These are often more polar than the classical persistent environmental pollutants and can betransported in the vascular system after having entered the plant. They are defined as systematic

pesticides. Binding of pesticides in the apoplastic pathway of stems showed, in a laboratory

experiment, to be related to their degree of lignification and to the hydrophobicity of the pesticides(Barak et al., 1983).

The main concern for human health regarding uptake of organic pollutants from soil is the risk of

contamination of agricultural fields and accumulation in crops. There are some studies of uptake of

environmental contaminatns present in sludge or compost (Beck et al., 1996; Kolb & Harms, 1996).These studies point in the same direction as earlier mentioned studies, no translocation through the

plant to edible parts above ground, but edible roots and tubers such as carrots can be contaminated.However, volatile compounds may contaminate edible leafs and fruits after volatilisation and

transport through the air. There is also the possibility that fruits and shoots near soil can be

contaminated directly by soil.

Roots provide anchorage and energy storage and undergo both physical and chemical interactionwith the soil. It is in many cases accurate to imagine as much of the plant below ground as above.

Considering differences between species and environmental conditions most roots actively modify

their environment in one way or another. The rhizosphere bacteria and fungi are nourished byorganic nutrients exuded from roots, some micro-organism contribute to plant health by modifying

soil acidity, adding chelating agents, producing antigens to ward of pathogens, and expanding the

effective absorption area resulting in increased water and nutrient uptake. Currently the informationregarding the mycorrhizal influence on uptake and chemical metabolism is insufficient.

Remediation

Plants and the associated microbial communities in the rhizosphere offer a potentially important

treatment strategy for biological remediation of chemically contaminated soils. Most experimentsshow degradation in soil by micro-organisms rather than uptake in plants as the main cause of

dissipation of organic chemical from the soil. Bioremediation is often facilitated in the rhizosphere

probably because of the ability of the roots to modify their environment (Todd et. al. 1993). There

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is, however, also possibility of bioaccumulation in plant that can be used to enhance remediation of

contaminated soils. Burken and Schnoor showed both uptake and metabolism of the herbicideatrazine in poplar trees (Populus) grown in bioreactor, but the seedlings were taken from 3-4 years

old trees (Burken & Schnoor, 1997). Adsorption of naphthalene by roots of two plant species (tall

fescue, Festuca arundinacea Schreber and alfa-alfa, Medicago sativa L.) with different lipidcontent has been quantified in a greenhouse experiment indicating that lipid content is a controlling

factor in adsorption of naphthalene onto plant roots (Schwab et al., 1998). Greenhouse experimentinvestigating the use of vegetation to increase degradation of anthracene and pyrene in soil (Reilley

et al., 1996).

Uptake from air

The waxy layer of cuticle serves as a barrier to water loss and a rate-limiting barrier for uptake of

xenobiotics into plant leaf cells. The cuticle consists predominantly of lipid material, synthesised by

epidermal cells and deposited on the outer surface. The cuticular membrane consists of an outerregion of soluble and polymerised aliphatic lipids and an inner layer containing large amount of

various cell-wall polysaccharides. A pectin-rich layer attaches the cuticular membrane to the cellwall. More or less all plant species also have an outer epicuticular wax layer. Principal component

of the cuticle membrane is the lipid polyester cutin. Cutin is an insoluble polyester of cross-linked

hydroxy-fatty acid and hydroxyepoxy-fatty acids and waxes the precise intermolecular structure isstill uncertain. Incorporated in the cutin are structures of fibrillae and lamellae. The fibrillae are

composed of polysaccharides, which may exhibit a distinctive reticulate pattern while lamellae maycontain wax compounds (Kirkwood, 1999).

Organic compounds can reach plant surface as free gas molecules, dissolved in water droplets, orsorbed to particles. Deposition from the gas phase or sorbed to particles is called dry deposition,

while deposition of contaminants dissolved in water is called wet deposition. The depositedcompounds can be incorporated in cuticular lipids, diffuse through the lipid layer and eventually be

translocated by phloem, or contaminants may enter the plant through stomata as a gas. It has been

suggested that beside the lipid component of the cuticle there also exist an aqueous route consisting

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of pores, carbohydrate strands and lipid interfaces (Price, 1982; Paterson et al., 1990). Welsch-

Pausch and co-workers (1995) found that dry gaseous deposition was the principal pathway of Cl4-Cl6 dioxins and furanes (PCDD/F) in greenhouse and out-door experiments with welsh ray grass

(Lolium multiflorum). Two similar field studies were made by Simonich and Hites and Nakajima

and co-workers(1994; 1995) concerning deposition of polycyclic aromatic hydrocarbons (PAH) to anumber of plant surfaces (needles, leaves, seeds, and bark from sugar maple (Acer saccarum) and

white pine trees (Pinus strobus) and azalea leaves (Rhododendron oomuraski)

Uptake from air into plants will be influenced by temperature, air pollutant concentration, plant

species and properties and content of lipids content, time of exposure, whether the pollutant is in thegas or particle phase and properties of the compound such as hydrophobicity, molar volume and

volatility.

Hydrophobicity is, as for other uptake routes, a very important factor for foliar uptake. In general

compounds of intermediate hydrophobicity, log Kow = 1-3, are taken up and translocated moreeasily through the cuticle than compounds outside this range, according to Trapp and McFarlane

(1995) Unlike in roots there are no endodermis for molecules to pass before reaching the transport

stream when compounds are applied to foliage and shoot thus allowing a more efficient movementof polar compounds. Translocation of hydrophobic compounds is limited by their sorption onto

plant solids including the cuticle itself. They are also less readily translocated via phloem transport

because of low or non-solubility. On the contrary is the large lipophilic surface that the plant foliageconstitutes an ideal collector for hydrophobic compounds. Surface sorption and uptake into needles

increased with hydrophobicity according to Schreiber and Schönherr (1992).

There is also some evidence for the influence of molar volume on uptake through plant leaves.

Bauer and Schönherr (1992) have correlated the solutes molar volume with the mobility in the outerlayer of the cuticle. The rate constants of desorption and the molar volume showed good

correlation. How size of solutes and temperature affect diffusion in plant cuticle was alsoinvestigated by Baur and co-workers (1997).

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The uptake rate and mobility of chemicals in cuticles from different plant species differ

considerably (Riederer & Schönherr, 1984; 1985; Keymeulen et al., 1993; McCrady, 1994; Baur et

al., 1997). The experiments of Riederer and Schönherr on the accumulation and transport of 2,4-

dichlorophenoxy acetic acid (2,4-D) in enzymatically isolated plant cuticles shows a wide variation

between species (Riederer & Schönherr, 1984; 1985). Content and composition of lipids and foliagearea can be species-specific properties influencing uptake. Some studies has suggested that

pollutant concentration and rate constants should be normalised to the lipid concentration of thevegetation or its surface area, especially when directly comparing different species and tissues

(Schreiber & Schönherr, 1992; McCrady, 1994; Simonich & Hites, 1994). A problem with this is

the difficulties to correctly determine lipid content in vegetation. Some lipophilic compounds inplants are volatile, others are hard or impossible to extract quantitatively. There is also to little

knowledge which lipids are important for uptake of organic pollutants. Uptake can of course also beaffected by the condition of the plants. Uptake of the herbicide 2,4-D in soybean is, e.g., influenced

by plant water status (Kogan & Bayer, 1996).

Temperature has in laboratory experiments shown to influence the partition coefficient for uptake in

foliage (Baur et al., 1997; Keymeulen et al., 1997). However partitioning of PCB between air andrye grass (Lolium multiflorum) in laboratory (using fugacity meter) showed that under

environmental conditions the temperature dependence of the partitioning coefficient did not

influence the plant concentration of most semivolatile organic compounds (SOC:s). The slowuptake/clearance kinetics prevents the plant/air system from reacting quickly to the new equilibrium

state resulting from the temperature-induced change in the partitioning coefficient. Simonich and

Hites (1994) defined a vegetation-atmosphere partition coefficient (Kv) that account for vegetationconcentration of semivolatile compounds (SOCs), the lipid content of vegetation and the

atmospheric gas-phase SOC concentration. They believe that the long-term partitioning is governedby gas-phase concentration and temperature and that there exists an annual cycle of partition of

SOCs into the waxy layer at low temperatures (in spring and fall) and a volatilisation back in the

summer. Also, Franzaring points out the temperature as the most important factor governingaccumulation of gas-phase organic air pollutants (Franzaring, 1997).

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Octanol-air partition coefficient, Koa, is a parameter used to understand the sorption of a pollutant to

leaf surfaces. Koa can be calculated from Henry´s law constant, H´, and Kow (Paterson et al., 1991)or measured (Harner & MacKay, 1995; Keymeulen et al., 1997). Harner made these measurements

by passing air saturated with octanol through a glass wool column coated with a solution of the

compound in octanol and measured the compound in the outlet air by collecting it on an absorbenttrap. The authors suggest that Koa be measured directly, especially for highly hydrophobic organic

compounds. They also showed that Koa is strongly dependent on temperature. Keymeulen and co-workers used a headspace method to determinate cuticle-air partition coefficient (Kca) for four

monocyclic hydrocarbons (benzene, toluene, ethylbenzene, m-, p-, and o-xylen) and showed good

correspondence between log Kca and log Koa. A laboratory study supports that plant-air partitioncoefficient is linearly correlated with Koa (Tolls & McLachlan, 1994).

Difference between measured (Riederer & Schönherr, 1984) and from determined permeance

(Riederer & Schönherr, 1985) calculated leaf-air partition coefficient gave the conclusion that the

cuticle membrane is not homogenous. According to Schönherr and Riederer cuticles areheterogeneous membranes and may be looked at as composite membranes made up of a thin outer

skin which is the barrier limiting rate of uptake and transport and an inner compartment which isresponsible for its sorptive properties (Schönherr & Riederer, 1989). Kinetics of uptake has been

described as a one-compartment model for the entire leaf. Bacci et. al has described uptake and

clearance of organic contaminants into azalea leaves in greenhouse experiments in a one-compartment model: the so called “azalea model” (Bacci et al., 1990b). More recent experiments

indicate that needle uptake are better described by a two-compartment model (Reischl et al., 1987;

Schreiber & Schönherr, 1992; Hauk et al., 1994; Tolls & McLachlan, 1994). Many authors havenoted that equilibrium may never be reached during the length of experiment (Paterson et al., 1991;

McCrady & Maggard, 1993; Hauk et al., 1994; Tolls & McLachlan, 1994; Umlauf et al., 1994;Hung et al., 2001). Selective solvent extraction methods have been developed to separate these two

compartments (Reischl et al., 1987; Hauk et al., 1994; Strachan et al., 1994; Umlauf et al., 1994). A

fast response to temperature and initial exposure has been found by Simonich et. al. and Nakajimaet. al. and are presumed to be due to accumulation by the outer leaf or needle compartment

(Simonich & Hites, 1994; Nakajima et al., 1995). Keymeulen and co-workers exposed virgin pinetrees to toluene, ethylbenzene, and xylen under field conditions for several years (Keymeulen et al.,

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1993). It took 5-6 month to reach equilibrium in most cases. This can be due to slow partitioning

into an inner leaf compartment .

Biomonitoring

Many studies have been made on using pollutant concentration in vegetation as indicators of

atmospheric contamination levels. This has been reviewed in some papers (Paterson et al., 1990;

Kylin, 1994; Simonich & Hites, 1995; Smith & Jones, 2000)There are advantages to use plants instead of ordinary air sampling. Vegetation integrates

contamination over time and is much easier and cheaper to collect than air samples. The use ofvegetation to qualitatively indicate organic pollutant atmospheric contamination is valid as long as

the mechanism of plant uptake is considered. Different species have been used for biomonitoring

persistent organic pollutants within cities, countries, continents, and on global basis. Scots pine(Pinus sylvestris) (Eriksson et al., 1989; Calamari et al., 1991; Jensen et al., 1992,Tremolada, 1996

#448; Safe et al., 1992; Strachan et al., 1994; Juuti et al., 1995), spruce (Picea abies), (Reischl,1988; Weiss, 1998) Saxifrage (Saxifraga oppositofolia) (France et al., 1997) are example of species

used and also for identifying point sources. Most studies on uptake from air are done on leaves or

needles but there are some studies on bark (Simonich & Hites, 1994).

Evergreen plants such as conifers are well suited for biomonitoring of persistent organic pollutantsboth on local, regional and global level. They can be sampled all year around and several year-

classes of needles can be found on the individual trees. Biomonitoring of organic contaminants with

conifers has been used to observe geographic and temporal patterns of atmospheric organicpollutants (Eriksson et al., 1989; Jensen et al., 1992; Tremolada et al., 1996; Weiss, 1998).

Conclusion drawn from those are that higher concentration in needles of the pesticides DDT andlindane (γ-hexachlorohexane [γ-HCH]) are found closer to spraying areas, α-hexachlorohexane (α-

HCH) is uniformly spread throughout Europe probably because of long-range transport and PCBand HCB in needles seems to be indicators of industrial activities. The accumulation of polycyclic

aromatic hydrocarbons (PAHs) in vegetation has been investigated in several studies (Kylin, 1994;Simonich & Hites, 1994; Wagrowski & Hites, 1997; Bakker, 2002). A preliminary Swedish

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investigation of 24 PAHs at 9 sites near Stockholm and two Estonian sites was performed in 1993

showing elevated concentration near roads and industries (Kylin, 1994). PAH burdens on a massper total leaf area were determined in urban, suburban and rural vegetation in northeastern USA to

quantify the ability to remove PAHs from air. PAH burdens in rural areas were on average 10 times

lower than in urban areas. The calculated PAH flow was 160 t /year from the atmosphere tovegetation. Vegetation scavenged about 4 % of the total amount of emitted PAH (Simonich &

Hites, 1994).

Sampling along a latitudinal transect on Ellesmore Island in the Canadian High Arctic (76°-83° N)

was undertaken to determine the most likely influx pathways of OC pollution to this region. Atseven sites the sums of six organchlorine groups (toxaphene, HCHs, CBz, Chlordane-related

compounds, DDT, PCB) was determined in saxifrage. The authors claim that they found a closerelationship between the OC concentrations and the plant cesium-137 activities. The r_ for the

relationships between OC concentrations and caesium activity ranged from 0.42 to 0.82 (France et

al., 1997)

Transport and metabolism

With exception of hormone-like chemicals, there is no evidence of active uptake and transport for

anthropogenic chemicals (Trapp & McFarlane, 1995). Passive uptake and transport is controlled bydiffusion, solubility in water and in the cuticular membrane. Generally, this can be explained by

physical properties such as hydrophobicity and acid strength affecting the reversible partitioning ofnonionised compounds onto the plant solids of the stem or the ion trapping in for example the

phloem for weak acids. Partitioning of chemicals to materials in the stem increases with increasing

Kow (McCrady et al., 1987). Metabolism is more difficult to predict and may differ markedlybetween species unlike the transport processes. Live cells, especially near the cambium and phloem,

may provide an area for rapid metabolic degradation of anthropogenic chemicals (Trapp &McFarlane, 1995)

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The most important property for transport of nonionised chemicals in plants is the hydrophobicity.

It determines the ease of movement across membranes. Partitioning of compounds onto plant solidslimits the long-distance transport and is also a function of hydrophobicity. Movement of nonionised

compounds is analogous with column chromatography. Briggs and co-workers defined a stem

concentration factor, SCF (Briggs et al., 1983)SCF=conc in stem/conc in external solution

He found the relationship:

log SCFmacerated stems = 0.95 log Kow - 2.05

Movement of 17 substituted benzenes , under pressure through stem segment of soybean, withtranspiration stream gave rice to accumulation at sites with the greatest transpiration in the shoot

(McCrady et al., 1987).

Movement from root to shot is described with the transpiration stream concentration factor TSCF

(Briggs et al., 1982) Determined analogous with RCF:

TSCF=conc in xylem sap/conc in external solution

usually estimated from measurements of the amount of compound accumulated for a known amount

of transpiration if necessary corrected for the degradation rate of the compound

TSCFcorrected=(TSCFapparent*t*k)/[1-exp(-kt)]

Briggs and co-workers have measured TSCF for two series of nonionised compounds (O-

methylcarbamoyloximer and phenylureas in barley) spanning over a wide range of Kow showing an

optimum at log Kow 1.8 (Briggs et al., 1982).

Other literature data also fit the curve reasonably well. Sicbaldi and co-workers also found aGaussian curve relationship when studying pesticides from different chemical classes in soybean

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although with the maximum at a Kow of approximately 3.0 (Sicbaldi et al., 1997). To reach the

vascular system compounds must pass the barrier between the apoplastic and symplastic system andTSCF is a measure of the ability to do this. Polar compound should have difficulties passing the

lipophilic membrane of endodermis and indeed TSCF is reduced as log Kow decrease. Why TSCF

also decrease when log Kow raise is not fully understood (Trapp & McFarlane, 1995). Partitioningonto lipid-like phases can be one explanation. Apparently more hydrophobic compounds cross the

endodermis much less efficient than water.

Nonionised compounds move more easily in the greater water flow in the xylem thus they can

move freely between the phloem and xylem tissue. The uptake of weak acids is pH dependent andthe polarity increases markedly for the ionised form of a compound. Therefore, the movement of

weak acids across the membranes can change with pH. Carboxylic acid having pKa values between3 and 6 produce anions typically 3 to 4 log Kow units more polar than the undissociated parent acids.

Therefore, the SCF for weak acids depends not only on Kow but also on pKa, the permeability ratio

(PAH/PA-) and on the pH of the xylem sap and the adjacent plant compartments and also TSCF forthose compounds is dependent on pH of the surrounding medium. For example Uptake of 2,4-D

with surrounding pH 4 gave a TSCF = 4.14 and at pH 7 TSCF = 0.04 (Briggs et al., 1987).

Because of the lipophilic membrane between

xylem and phloem and the much greater volumeof flow (50- to 100-fold) in the xylem the

majority of phloem-mobile xenobiotics are weak

acids. Polar nonionised compounds do not crossthe membrane and the hydrophobic compounds

cross the membrane but diffuse back into thegreater volume of xylem. Weak acids accumulate

in the phloem by ion trapping in the more basic

phloem (pH~8) relative to the apoplast (pH ~5.5)(fig 4). Transport in the phloem depending on

two processes first the compound need to enter the phloem through the membrane and then betransported effectively in the phloem. For optimal diffusion into phloem the acid should be as

AH

10 A-

apoplast, pH = 5.0 phloem sieve tube, pH = 8.0

Figure 4. Accumulation of weak acids within cellsby the ion trap effect. From (Trapp & McFarlane,1995).

10000 A-

AH

23

undissociated as possible (high pKa) and the undissociated molecule ought to have log Kow ~1.8.

But to remain and be transported long distances in the phloem, the compounds should have a lowpKa and the small amount of undissociated molecules should be very polar log Kow < 1 to remain in

the phloem.

One of the compounds shown to be transported most efficiently is maleic hydrazide (Trapp &

McFarlane, 1995). The pKa of maleic hydrazide is 5.65, which is almost optimum for accumulation.On the other hand, the log Kow is -0.63, optimal for remaining in phloem. Glyphosate, a common

herbicide, is also translocated extremely well in the phloem. This is a complex compound with three

acidic functions and one basic amino group.

Metabolism in plants resembles liver metabolism in many ways and oxidation is the mostfrequently observed transformation reaction. Reductive processes are less common, hydrolytic

reactions may also occur. Conjugation takes place in two ways. Soluble conjugates can be formed

introducing glucoside, gluthatione, amino acid or malonyl to the functional group existing in thexenobiotics or formed in the transformation reaction. Incorporation in biomolecules gives insoluble

or bound conjugates. Many aromatic or heteroaromatic compounds with hydroxyl, carboxyl, aminoor sulfhydroxyl groups are known to be deposited into lignin or other cell wall components. The

basic different between plant and liver metabolism is that conjugates are predominantly excreted in

animals but in plants they are compartmentalised and stored within plant tissue (Trapp &McFarlane, 1995).

The OH- derivatives of atrazine seems to represent the greater part of the metabolites developed bycorn seedlings The parent compound transformed very readily after entering the seedling (Raveton

et al., 1997). An outdoor pot study by Nakagawa et. al. also concluded that hydroxyatrazin was themain metabolite (Nakagawa et al., 1996). The pyrimidyl moiety of the fungicide cyprodinil (4-

cyclaopropyl-6-methyl-2-(phenylamino)pyrimidin was shown to be taken up more readily then the

phenyl part when studying soil-bound residues of 14C-labelled compound in methanol-extracted soil(Dec et al., 1997). Harms (1992) compared the phytotoxicity and metabolic fate of pesticides in cell

cultures of plants and seedlings grown under aseptic conditions and concluded that the metabolites

24

were qualitatively the same. A study of uptake and transformation of benzene and toluene by plant

leaves with a similar method was made by Ugrekehelidze (1997).

Methods

The focus of research on plant uptake has been on laboratory studies and comparatively fewer field

studies have been done. There are methods developed for cell cultures and ground plant parts(Langebartels & Harms, 1985; Harms, 1992; Raveton et al., 1997), and separate plant parts like

cuticles or leaves (Barak et al., 1983; Riederer & Schönherr, 1984; Langebartels & Harms, 1985;Riederer & Schönherr, 1985; Schönherr & Riederer, 1989; Bauer & Schönherr, 1992; Keymeulen et

al., 1997; Kömp & McLachlan, 1997). Other have developed advanced laboratory system to study

whole plants (Topp et al., 1989; McCrady et al., 1990; Trapp et al., 1990; Schroll & Scheunert,1992; Hauk et al., 1994; Tolls & McLachlan, 1994; Sicbaldi et al., 1997), or greenhouse and

outdoor pot and lysimeter experiment (Fries & Marrow, 1981; Bacci & Gaggi, 1985; 1986; Bacci

et al., 1990a; Bacci et al., 1990b; Bacci & Calamari, 1991; Bacci et al., 1992). Cell cultures is oftenused for studies of metabolism in plant cells (Harms, 1992; Raveton et al., 1997). Harms made a

comparing study of phytotoxicity and metabolic fate of pesticides in cell cultures of plants andseedlings grown under aseptic conditions. Advantages of using cell cultures are the cost counted in

time and equipment compared to growing whole plant under controlled conditions. It is easy to

make repeated experiments and the answers are quick and rather free from disturbing factors. Thereis no competing metabolism by micro-organism and it is easy to control photodegradation. The

major drawback is that we do not get the whole picture. Metabolism in a mature plant or a seedlingcan differ greatly from that in a cell culture. Langebartel et.al.(1985) used a fractionating procedure

with both chemical and enzymatic method to investigate residues of pentachlorophenol bound to

different cell wall compartments. Barak and co-workers used ground stems to relate binding ofpesticides to lignification and to hydrophobicity of the pesticides (Barak et al., 1983).

Riederer and co-workers using enzymatically isolated cuticles to investigate adsorption transport

and permeability in plant leaves. Some of the experiments are repeated with the polymer matrix left

after extraction of the soluble cuticular lipids (Riederer & Schönherr, 1984; 1985). Schönherr and

25

Bauer presented a technique to measure the unilateral sorption from the outer face of an isolated

cuticle (Schönherr & Baur, 1996). The apparatus used was a desorption chamber and a lid betweenwhich the cuticular membrane was sandwiched (Schönherr & Riederer, 1989). Determination of the

plant cuticle-air partitioning coefficients with enzymatically isolated cuticles was made by

(Keymeulen et al., 1997). The method was based on gas phase equilibrium of target compound inclosed vials and their analysis by headspace gas chromatography.

The fugacity meter described by Kömp and McLachlan measures the concentration of a chemical

in air in equilibrium with a solid phase (Kömp & McLachlan, 1997). It consists of a glass column in

which the plant material is packed. An air stream is then passed through the column in such a waythat equilibrium between the surface of the vegetation and the air is established. In this way the

equilibrium partitioning can be measured after only brief periods of contamination since theequilibrium of SOCs within the plant is much more rapid than the transport to the plant .

Many studies have been made on uptake by the roots of the whole plant and subsequenttranslocation in the xylem and the strategy usually are to apply the xenobiotics in nutrient solution

and measure the amount collected in different parts of the plant. Sicbaldi and co-workers measuredconcentration of pesticides directly in xylem sap collected from stem or leaf bases using pressurised

root chamber (Sicbaldi et al., 1997).

When investigation the pathways of organic pollutant into plants it is often needed to separate the

air movement from soil to foliage from the systemic transport from root to leaf. Schroll et. al.

present a closed laboratory system consisting of a modified desiccator that make it possible toseparate determination of both plant pathway as well as a complete mass balance of 14C (Schroll &

Scheunert, 1992). It is a further development of the, by Topp and co-workers, earlier usedequipment (Topp et al., 1986). McCrady and co-workers separated shoots from the roots and the

hydroponic solution in exposure chambers consisting of two canning jars one inverted over the

other (1990).

Something in between laboratory and field studies are outdoor lysimeter experiments includingsimulation of climate soil and biotic parameters. Bacci and co-workers (1985; 1986; 1990a; 1990b;

26

1991; 1992) used greenhouse with controlled air flux temperature and light for study of uptake and

release kinetics organic compounds in azalea leaves. Outdoor pot experiments with contaminatedsoils have for instance been done by Nakagawa and co-workers and by Fries and Marrow (1981;

1996). Hülster and co-workers designed field experiment on contaminated soil with conventionally

grown zucchini, fruits grown without soil contact, plants grown in pots with uncontaminated soilburied in the contaminated soil so that fruits and low growing leaves are in contact with

contaminated soils, and plant grown in uncontaminated soil 1.5 m above ground (1994)

Studies of seedling can be misleading and caution should therefore be observed when modelling

and considering seedling experiments for verification of modelling results. In growing seedlingmost development occurs in the roots, materials and energy are derived from the seed,

photosynthesis and transpiration are often very limited, biochemical reaction differ dramaticallyfrom those of mature plants.

Photodegradation and volatilisation on plant surface should be taken into consideration when

studying plant uptake. Volatilisation chambers can be used for determining the volatility ofpesticides from plant surfaces (Starr & Johnson, 1968; Dörfler et al., 1991)

The distribution is normally measured by autoradiography following application of radiolabeledcompounds (Fries & Marrow, 1981; Briggs et al., 1982; Briggs et al., 1983; Langebartels & Harms,

1985; Topp et al., 1986; Scheunert et al., 1989; Schroll & Scheunert, 1992; Dec et al., 1997). One

disadvantage with this technique is that it shows only the position of the radiolabel and does notidentify the compound. A way to achieve more information is to labelling different parts of the

molecule as Dec did when studying cyprodinil uptake from soil into barley (Dec et al., 1997).

Some field studies are made on uptake mechanism. Reischl et. al. analysed distribution of DDT

DDE α-and γ-HCH, HCB in spruce needles sampled in northern Bavaria. They compared the

content in the wax with that in the remaining of the needle concluding that DDT and DDE stays inouter of the needle and HCH an HCB are also found inside the needle (Reischl et al., 1987). Umlauf

et. al. confirmed this by exposing spruce needles with PCBs DDT, DDE, tetra- penta- and

hexachlorobensen, and α-and γ-HCH in laboratory chambers (Umlauf et al., 1994). Compounds

with higher molecular weights (PCBs, DDT and DDE) were easily extracted from the needles whilethe compounds with lower molecule weight (chlorobenzenes and HCHs) seem to penetrate into the

27

interior of the needle and took longer time to extract. Kylin et. al. evaluated a method with longer

extraction time for the outer compartment (Kylin et al., 1996). However, it should be rememberedthat the definition of the outer and inner compartments of needles or leaves can only be made

operationally and that no absolute definition is, as yet, possible. One possible biochemical

definition of three compartments is, 1) the epicuticular wax 2) the cuticle lipids 3) the inner lipids ofthe needle .

Strachan and co-workers sampled pine needles along a transect from northern Norway to southern

West Germany (Strachan et al., 1994). They compared calculation of concentration on area basis

with calculation on fresh weight basis. Water content was almost the same in all samples and thetwo calculations gave similar interpretations. They also studied sampling methodology and found

that the number of sampled trees and the age of the trees are not important factors, the facingdirection might be of concern if local sources exist but the sample height of the trees is an important

factor. A comparison of using dry weight or lipid weight as basis for PAH concentrations in a

number of plant parts, among them pine needles, during the growing season showed that the lipidconcentration had a large effect on PAH concentration, especially in needles (Simonich & Hites,

1994). On the other hand the lipids in needles and other plant parts are very diverse regardingphysical and chemical properties. Therefore, measuring the amount of them can be difficult and

also to know which of them that are important for the uptake.

Models

Because of the large number of organic compounds present in the environment there are tools

needed for interpretation and prediction of the fate of chemicals in plants. One possibility to achieve

this is mathematical models that combine the physiochemical properties of chemicals withanatomical and physiological properties of plants. Models have been developed to integrate

available knowledge of the complex interactions and to aid in presentation of plant functions andhelp make predictions about chemical fate. There is everything from simple mathematical

relationship to advanced models consisting of several compartments. There are model taking the

whole plant into consideration (Trapp et al., 1990; Dowdy D & McKone T, 1997; Hung & Mackay,

28

1997) and those modelling specific parts, for instance uptake in cuticle/leaves (Paterson et al., 1991;

Tolls & McLachlan, 1994; Deinum et al., 1995)

Ryan et.al presents a procedure to group chemicals for their relative potential for plant uptake on

their chemical and physical properties (Ryan et al., 1988). Dowdy and McKone predicts plantuptake from calculated molecular connectivity index (Dowdy D & McKone T, 1997).

Many models are based on fugacity. Fugacity is a compounds tendency to “flee” a system (from

Latin fugere, to flee) (Schwarzenbach, 1993). It is a way to describe a relative chemical potential of

a compound in a system. When a compound is in equilibrium between two phases in theenvironment the concentration differ in the two media but the fugicity is the same. Fugacity

quotients are used to studying food chain bioaccumulation (McLachlan, 1996). The approach is todivide the fugicity of a compound in the organism by the fugicity of the surrounding phase.

Fugacity f, with unit of pressure (Pa), is an equilibrium criterion which is linearly related to

concentration C (mol*m-3) through a fugacity capacity Z (mol*m-3*Pa-1), where:

C=Zf

The difference between using partitioning coefficient and fugacity is only the formulation.

A three-compartment (leaf, stem and root) fugacity model applied on bromacil in soybean under

hydroponic conditions was presented by Hung and McKay (1997). The model is believed to give

acceptable accurate prediction for risk assessment of exposure to contaminants consumed eitherdirectly from vegetation or indirectly in natural and agricultural food chains.

A methodology for assessing congener-specific vapour-particle partitioning and photolytic

degradation rates of dioxin and dioxin-like compounds and to assess environmental concentration

associated with uptake of vapour phase chemicals by plants was presented by Chrostowski and co-workers (1996).

29

Reflections and future research

Uptake of organic compounds in plants is a large area of research with many aspects to consider.

Contamination of agricultural crops and the possible accumulation in the food chain is the riskscenario most people find alarming because it concerning human health directly. There is also the

ecotoxicological aspect. Organic pollutant can affect plants when taken up. Accumulated chemicals

can reach soil when the plant wilt and disturb the microbial ecosystem or reach the ground water.Plants probably play an important roll in long rang air transport of semivolatile organic compounds

over terrestrial areas.

Bioconcentration in plants can be of use for other purposes. Remediation of contaminated soils can

be achieved to some extent by uptake in plants even if most of the effect seen is due tomicrobiological degradation. Plants, and especially evergreen conifers, can be used for

biomonitoring concentration and movement of semivolatile organic compounds in air.

The large amount of chemicals and plant species make it impossible to analyse every combination

especially taking different environmental factors into account. The large diversity of speciesconcerning such as lipid content, foliage and root area, metabolism and other biochemical

properties and the large diversity of chemical properties among the organic pollutant make it hard to

find generally applicable relationships to predict the fate of organic compounds in plants. Upon thatthe diversity of the whole environment must be taken into account. However with our knowledge

about physical and chemical properties of different chemical classes and physiology andbiochemistry of plants in combination with experimental experience we can make some predictions

about possible scenarios.

It seems that most effort has been put on laboratory experiments and in most research areas

concerning uptake in plants more field studies are needed. Details of mechanism are often betterstudied in controlled laboratory experiments, but the experience of field studies is needed to fully

understand the broad relationships.

30

In the field of uptake from soil one of the most interesting research result is the discovery of

translocation of dioxins in members of the genus Cucurbita. The uptake and possible translocationof hydrophobic compounds in pumpkins and zucchini and related species should be further studied.

Both if there is some genus specific transport system and if other species or other hydrophobic

compounds show the same behaviour.

An interesting research area according to uptake from air is the use of plants as biomonitors. Largecontinuous programs to monitor organic air pollutants are expensive. A great deal of the cost is

field-sampling equipment. If it were possible to use the natural sampling surface that evergreen

conifers constitutes it would be feasible to monitor larger areas. There is, however, a need to studythe mechanisms more thorough to know if we get a momentous picture or a long-term sampling

when we analyse the plants.

Furthermore it is necessary to keep up with the release of new chemicals. The brominated flame

retardants are, among others, a new source of alarm. Those are for instance found in sludge spreadon the fields and it is easily claimed that those hydrophobic compounds are not taken up in the

crops. There are, as we have seen, possible that some plants translocate even very hydrophobiccompounds to eatable parts and there are several evidences that lipid-rich roots like carrots

accumulate hydrophobic compounds.

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